Skip to main content

Advertisement

SpringerLink
Log in

Circulating microRNA-22-3p Predicts the Malignant Progression of Precancerous Gastric Lesions from Intestinal Metaplasia to Early Adenocarcinoma

  • Original Article
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Background

Gastric cancer has a poor outcome and identifying useful biomarkers from peripheral blood or tissue could allow its early detection, or potentially precancerous changes, thus improving the curative rates. MicroRNAs (miRNAs) have been shown to offer great potential in cancer diagnosis and prediction.

Aim

Here, we investigated the role of plasma miRNAs in the natural course of gastric cancer, from intestinal metaplasia to early cancer. The findings were used to understand whether patients at a high risk of malignancy could be given appropriate interventions in the early disease process, such as using endoscopic submucosal dissection to treat gastric dysplasia or early gastric cancer.

Methods

Participants were divided into healthy control, intestinal metaplasia (IM), and dysplasia/early cancer (pT1a/b) groups. Microarray was used to select potential markers in tissue.

Results

Quantitative real-time polymerase chain reaction data showed circulating miRNA-22-3p had significantly different expression in patients with precancerous lesions or gastric adenocarcinoma. The areas under the curve of incomplete IM versus healthy control, low-grade/high-grade dysplasia, early gastric cancer, and GED were 0.8080, 0.8040, 0.8494, and 0.8095, respectively (all P values < 0.05).

Conclusions

Circulating miRNA-22-3p could be a potential biomarker for gastric precancerous dysplasia and early cancer detection.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Brenner H, Rothenbacher D, Arndt V. Epidemiology of stomach cancer. Methods Mol Biol. 2009;472:467–477.

    Article  PubMed  Google Scholar 

  2. Karpeh M, Kelsen D, Tepper J. Cancer of the stomach. In: DeVita V, Hellman S, Rosenberg S, eds. Cancer Principles & Practice of Oncology. Philadelphia: Lippincot, Williams & Wilkins; 2001:1092–1126.

    Google Scholar 

  3. Sugano K. Detection and management of early gastric cancer. Curr Treat Options Gastroenterol. 2015;13:398–408.

    Article  PubMed  Google Scholar 

  4. Kanzaki H, Takenaka R, Kawahara Y, et al. Linked color imaging (LCI), a novel image-enhanced endoscopy technology, emphasizes the color of early gastric cancer. Endosc Int Open. 2017;5:E1005–E1013.

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rugge M, Pennelli G, Pilozzi E, et al. Gastritis: the histology report. Dig Liver Dis. 2011;43:S373–S384.

    Article  PubMed  Google Scholar 

  6. Leung WK, Wu MS, Kakugawa Y, et al. Screening for gastric cancer in Asia: current evidence and practice. Lancet Oncol. 2008;9:279–287.

    Article  PubMed  Google Scholar 

  7. Marrelli D, Roviello F, De Stefano A, et al. Prognostic significance of CEA, CA 19-9 and CA 72-4 preoperative serum levels in gastric carcinoma. Oncology. 1999;57:55e62.

    Article  Google Scholar 

  8. Esquela-Kerscher A, Slack FJ. Oncomirs—microRNAs with a role in cancer. Nat Rev Cancer. 2006;6:259–269.

    Article  PubMed  CAS  Google Scholar 

  9. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006;6:857–866.

    Article  PubMed  CAS  Google Scholar 

  10. Kosaka N, Iguchi H, Ochiya T. Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 2010;101:2087–2092.

    Article  PubMed  CAS  Google Scholar 

  11. Mitchell PS, Parkin RK, Kroh EM, et al. Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci USA. 2008;105:10513–10518.

    Article  PubMed  Google Scholar 

  12. Tsujiura M, Ichikawa D, Komatsu S, et al. Circulating microRNAs in plasma of patients with gastric cancers. Br J Cancer. 2010;102:1174–1179.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Tsai MM, Wang CS, Tsai CY, et al. Circulating microRNA-196a/b are novel biomarkers associated with metastatic gastric cancer. Eur J Cancer. 2016;64:137e148.

    Article  CAS  Google Scholar 

  14. Correa P. Human gastric carcinogenesis: a multistep and multifactorial process—first American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res. 1992;52:6735–6740.

    PubMed  CAS  Google Scholar 

  15. Busuttil RA, Boussioutas A. Intestinal metaplasia: a premalignant lesion involved in gastric carcinogenesis. J Gastroenterol Hepatol. 2009;24:193–201.

    Article  PubMed  CAS  Google Scholar 

  16. Correa P, Piazuelo MB, Wilson KT. Pathology of gastric intestinal metaplasia: clinical implications. Am J Gastroenterol. 2010;105:493–498.

    Article  PubMed  PubMed Central  Google Scholar 

  17. González CA, Pardo ML, Liso JM, et al. Gastric cancer occurrence in preneoplastic lesions: a long-term follow-up in a high-risk area in Spain. Int J Cancer. 2010;127:2654–2660.

    Article  PubMed  CAS  Google Scholar 

  18. Oka S, Tanaka S, Kaneko I, et al. Advantage of endoscopic submucosal dissection compared with EMR for early gastric cancer. Gastrointest Endosc. 2006;64:877–883.

    Article  PubMed  Google Scholar 

  19. Gotoda T. Endoscopic submucosal dissection of early gastric cancer. Curr Opin Gastroenterol. 2006;22:561–569.

    Article  PubMed  Google Scholar 

  20. Salvon-Harman JC, Cady B, Nikulasson S, Khettry U, Stone MD, Lavin P. Shifting proportions of gastric adenocarcinomas. Archives of surgery (Chicago, Ill: 1960). 1994;129:381–388. (discussion 388–389).

    Article  CAS  Google Scholar 

  21. Park JC, Lee YC, Kim JH, et al. Clinicopathological aspects and prognostic value with respect to age: an analysis of 3,362 consecutive gastric cancer patients. J Surg Oncol. 2009;99:395–401.

    Article  PubMed  Google Scholar 

  22. Petrelli F, Berenato R, Turati L, et al. Prognostic value of diffuse versus intestinal histotype in patients with gastric cancer: a systematic review and meta-analysis. J Gastrointest Oncol. 2017;8:148–163.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Slattery ML, Herrick JS, Pellatt DF, et al. MicroRNA profiles in colorectal carcinomas, adenomas and normal colonic mucosa: variations in miRNA expression and disease progression. Carcinogenesis. 2016;37:245–261.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  24. Bosman FT, Carneiro F, Hruban RH, Theise ND, eds. WHO Classification of Tumours of the Digestive System. 4th ed. Lyon: IARC Press; 2010.

    Google Scholar 

  25. Lin YH, Wu MH, Liao CJ, et al. Repression of microRNA-130b by thyroid hormone enhances cell motility. J Hepatol. 2015;62:1328–1340.

    Article  PubMed  CAS  Google Scholar 

  26. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods. 2001;25:402–408.

    Article  PubMed  CAS  Google Scholar 

  27. Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011;39:7223–7233.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Correa P. Clinical implications of recent developments in gastric cancer pathology and epidemiology. Semin Oncol. 1985;12:2–10.

    PubMed  CAS  Google Scholar 

  29. Kim J-W, Jang JY. Optimal management of biopsy-proven low-grade gastric dysplasia. World J Gastrointest Endosc. 2015;7:396–402.

    Article  PubMed  PubMed Central  Google Scholar 

  30. Wang W, Li F, Zhang Y, et al. Reduced expression of miR-22 in gastric cancer is related to clinicopathologic characteristics or patient prognosis. Diagn Pathol. 2013;8:102.

    PubMed  PubMed Central  Google Scholar 

  31. Zuo QF, Cao LY, Yu T, et al. MicroRNA-22 inhibits tumor growth and metastasis in gastric cancer by directly targeting MMP14 and Snail. Cell Death Dis. 2015;6:e2000.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Tang Y, Liu X, Su B, et al. microRNA-22 acts as a metastasis suppressor by targeting metadherin in gastric cancer. Mol Med Rep. 2015;11:454–460.

    Article  PubMed  CAS  Google Scholar 

  33. Wang G, Shen N, Cheng L, et al. Downregulation of miR-22 acts as an unfavorable prognostic biomarker in osteosarcoma. Tumor Biol. 2015;36:7891–7895.

    Article  CAS  Google Scholar 

  34. Li B, Song Y, Liu TJ, et al. miRNA-22 suppresses colon cancer cell migration and invasion by inhibiting the expression of T-cell lymphoma invasion and metastasis 1 and matrix metalloproteinases 2 and 9. Oncol Rep. 2013;29:1932–1938.

    Article  PubMed  CAS  Google Scholar 

  35. You Y, Tan JX, Dai HS, et al. MiRNA-22 inhibits oncogene galectin-1 in hepatocellular carcinoma. Oncotarget. 2016;7:57099–57116.

    PubMed  PubMed Central  Google Scholar 

Download references

Funding

This work was supported by a grant from Chang Gung Memorial Hospital, Taoyuan, Taiwan (CMRPG3D1392).

Author information

Authors and Affiliations

  1. Department of Gastroenterology and Hepatology, Linkou Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Taoyuan, Taiwan

    Tsung-Hsing Chen, Cheng-Tang Chiu, Yin-Yi Chu & Hao-Tsai Cheng

  2. Graduate Institute of Clinical Medical Sciences, Chang Gung University, Taoyuan, Taiwan

    Tsung-Hsing Chen

  3. Department of Industrial Engineering and Management, Yuan Ze University College of Engineering, Chung-Li City, Taiwan

    Chieh Lee

  4. Department of Surgery, Linkou Chang Gung Memorial Hospital, Chang Gung University College of Medicine, 259 Wen-hwa 1 Road, Taoyuan, Taiwan

    Jun-Te Hsu & Ta-Sen Yeh

  5. Department of Pathology, Linkou Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Taoyuan, Taiwan

    Ren-Chin Wu

  6. Graduate Institute of Biomedical Sciences, School of Medicine, Chang Gung University, Taoyuan, Taiwan

    Kwang-Huei Lin

  7. Liver Research Center, Linkou Chang Gung Memorial Hospital, Taoyuan, Taiwan

    Kwang-Huei Lin

  8. Research Center for Chinese Herbal Medicine, College of Human Ecology, Chang Gung University of Science and Technology, Taoyuan, Taiwan

    Kwang-Huei Lin

Authors
  1. Tsung-Hsing Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng-Tang Chiu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chieh Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yin-Yi Chu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hao-Tsai Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jun-Te Hsu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ren-Chin Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ta-Sen Yeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Kwang-Huei Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

THC, CTC, YYC, HTC, JTH, RCW, TSY, and KHL contributed to study concept and design. THC and CL involved in acquisition, analysis, and interpretation of data. THC drafted the manuscript. CL performed statistical analysis.

Corresponding authors

Correspondence to Ta-Sen Yeh or Kwang-Huei Lin.

Ethics declarations

Conflict of interest

The authors declare no conflicting financial interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 12 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, TH., Chiu, CT., Lee, C. et al. Circulating microRNA-22-3p Predicts the Malignant Progression of Precancerous Gastric Lesions from Intestinal Metaplasia to Early Adenocarcinoma. Dig Dis Sci 63, 2301–2308 (2018). https://doi.org/10.1007/s10620-018-5106-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-018-5106-4

Keywords

Search

Navigation